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The Evolutionary and Phylogeographic History of Woolly Mammoths: a Comprehensive Mitogenomic Analysis

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The Evolutionary and Phylogeographic History of Woolly Mammoths: a Comprehensive Mitogenomic Analysis www.nature.com/scientificreports OPEN The evolutionary and phylogeographic history of woolly mammoths: a comprehensive Received: 21 September 2016 Accepted: 10 February 2017 mitogenomic analysis Published: 22 March 2017 Dan Chang1,*, Michael Knapp2,*, Jacob Enk3,*, Sebastian Lippold4, Martin Kircher5, Adrian Lister6, Ross D. E. MacPhee7, Christopher Widga8, Paul Czechowski9, Robert Sommer10, Emily Hodges11, Nikolaus Stümpel12, Ian Barnes6, Love Dalén13, Anatoly Derevianko14, Mietje Germonpré15, Alexandra Hillebrand-Voiculescu16, Silviu Constantin16, Tatyana Kuznetsova17, Dick Mol18, Thomas Rathgeber19, Wilfried Rosendahl20, Alexey N. Tikhonov21,22, Eske Willerslev23,24,25, Greg Hannon26, Carles Lalueza-Fox27, Ulrich Joger12, Hendrik Poinar3, Michael Hofreiter28 & Beth Shapiro1 Near the end of the Pleistocene epoch, populations of the woolly mammoth (Mammuthus primigenius) were distributed across parts of three continents, from western Europe and northern Asia through Beringia to the Atlantic seaboard of North America. Nonetheless, questions about the connectivity and temporal continuity of mammoth populations and species remain unanswered. We use a combination of targeted enrichment and high-throughput sequencing to assemble and interpret a data set of 143 1Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, CA 95064, USA. 2Department of Anatomy, University of Otago, 270 Great King Street, Dunedin 9016, New Zealand. 3McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, 1280 Main Street West, Hamilton, Ontario L8S 4L9, Canada. 4Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig D04103, Germany. 5Department of Genome Sciences, University of Washington, 3720 15th Ave NE, Seattle, WA 98195-5065, USA. 6Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK. 7Department of Mammalogy, American Museum of Natural History, 200 Central Park West, New York NY, 10024, USA. 8Center of Excellence in Paleontology, East Tennessee State University, 1212 Sunset Dr., Gray, TN 37615, USA. 9Antarctic Biological Research Initiative, 31 Jobson Road, SA 5110, Australia. 10Department of Zoology, Institute of Biosciences, University of Rostock, Universitätsplatz 2, Rostock D-18055, Germany. 11Department of Biochemistry, Vanderbilt University School of Medicine, 2215 Garland Ave, Nashville, TN 37232, USA. 12Staatliches Naturhistorisches Museum Braunschweig, Pockelstrasse 10, Braunschweig 38106, Germany. 13Swedish Museum of Natural History, Department of Bioinformatics and Genetics, S-104 05 Stockholm, P.O. Box 50007, Sweden. 14Institute of Archaeology and Ethnography, Siberian Branch, Russian Academy of Sciences, 17, Novosibirsk, Akademia Lavrentieva, 630090, Russia. 15Operational Directorate “Earth and History of Life”, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, Brussels 1000, Belgium. 16“Emil Racoviţă” Institute of Speleology, Frumoasă 31, Bucharest, 01906, Romania. 17Department of Palaeontology, Faculty of Geology, Moscow State University, ul. Leninskiye Gory, 1, Moscow, 119991, Russia. 18Mammuthus Club International, Gudumholm 41, Hoofddorp, HG 2133, Netherlands. 19Staatliches Museum für Naturkunde Stuttgart Rosenstein, Gewann 1, Stuttgart 70191, Germany. 20Department “World Cultures and Environment”, Reiss-Engelhorn-Museen, C 5, Zeughaus, Mannheim, 68159, Germany. 21Zoological Institute Russian Academy of Sciences, Universitetskaya nab., 1 Saint- Petersburg 199034, Russia. 22Institute of Applied Ecology of the North, North-Eastern Federal University, Lenina 1, Yakutsk, Russia. 23Centre for GeoGenetics, Copenhagen University, Nørregade ‘10, Copenhagen, 1165, Denmark. 24Department of Zoology, University of Cambridge, Downing St. Cambridge, CB2 3EJ, UK. 25Sanger Institute, Wellcome Trust Genome Campus, Hinxton, CB10 1SA, UK. 26CRUK Cambridge Institute, University of Cambridge, Robinson Way, Cambridge, CB2 0RE, UK. 27Institute of Evolutionary Biology (CSIC-UPF), Doctor Aiguader, 88, Barcelona, 08003, Spain. 28Department of Mathematics and Natural Sciences, Evolutionary Adaptive Genomics, Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, Potsdam, 14476, Germany. *These authors contributed equally to this work. Correspondence and requests for materials should be addressed to B.S. (email: [email protected]) SCIENTIFIC REPORTS | 7:44585 | DOI: 10.1038/srep44585 1 www.nature.com/scientificreports/ mammoth mitochondrial genomes, sampled from fossils recovered from across their Holarctic range. Our dataset includes 54 previously unpublished mitochondrial genomes and significantly increases the coverage of the Eurasian range of the species. The resulting global phylogeny confirms that the Late Pleistocene mammoth population comprised three distinct mitochondrial lineages that began to diverge ~1.0–2.0 million years ago (Ma). We also find that mammoth mitochondrial lineages were strongly geographically partitioned throughout the Pleistocene. In combination, our genetic results and the pattern of morphological variation in time and space suggest that male-mediated gene flow, rather than large-scale dispersals, was important in the Pleistocene evolutionary history of mammoths. Late Pleistocene mammoth remains are common across Eurasia and North America in temperate as well as high latitude areas1,2. However, until recently, little effort was applied to the recovery of ancient DNA (aDNA) from fossils collected in mid-continental areas, as preservation of genetic material in these regions is generally much poorer than in high-latitudes. Gradual improvements in methodology and instrumentation have enabled recov- ery of aDNA from more challenging remains, such as from mammoth bones preserved in temperate regions of Eurasia3–5 and, more recently, North America6. These data can be used to resolve persisting questions regarding mammoth diversity and population structure. Our understanding of the evolutionary history of Mammuthus has been developed largely from mor- phological study of their fossils, especially the most resilient and therefore most abundant elements: molar teeth1,7–10. According to the fossil evidence, mammoths evolved in Africa during the late Miocene and later dis- persed into Asia and Europe, and eventually North America via Beringia, during the Middle Pliocene to Early Pleistocene1,10,11. The evolution of Mammuthus during the Pleistocene is usually presented as a succession of chronologically overlapping species, including (from earliest to latest) M. meridionalis (southern mammoths), M. trogontherii (steppe mammoths), and M. columbi (Columbian mammoths) and M. primigenius (woolly mammoths)1,7,8,10. According to the current model based on morphology, a population of southern mammoths gave rise to the steppe mammoth around ~1.7 million years ago (Ma) in Asia. Later, perhaps as early as 0.7 Ma, a second tran- sition occurred in Asia as a steppe mammoth population gave rise to the woolly mammoth1,12. Subsequently, these species dispersed out of Asia into Europe and North America. The European fossil record suggests sev- eral distinct waves of dispersal into Europe, after which the migrants may have coexisted and even hybridized with endemic European mammoth populations2,8. Until recently, it was generally held that southern mammoths dispersed into North America around 1.5 Ma13, where they evolved into Columbian mammoths (M. columbi), Jefferson’s mammoth (M. jeffersonii) and the Channel Islands pygmy mammoth (M. exilis)6,7. However, Lister and Sher2 recently suggested that southern mammoths never migrated to North America, and that all early North American mammoth fossils (1.5–1.3 Ma) that are classifiable based on morphology descend from dispersal(s) of steppe mammoths. A key implication of this interpretation is that the steppe mammoth population in northeast- ern Siberia was ancestral to both Columbian and woolly mammoths although at different points in time. Results of a recent study6 analysing complete mitogenomes from North American mammoth populations were consist- ent with this hypothesis. Furthermore, this study found evidence of hybridisation and potential male mediated gene flow between North American woolly mammoths, Columbian mammoths, Jefferson’s mammoth and pygmy mammoth6. Eurasian mammoths have received far less attention thus far. Previous population-level genetic analyses beyond the permafrost regions of Western Beringia were restricted to a small fragment of the mitochondrial genome. These studies partitioned woolly mammoth mitochondrial diversity into either three major clades3,5 or five haplogroups4 but were unable to resolve either the order in which these clades emerged or the timing of their origin. As a result the evolution of mammoths across their vast Eurasian range remains unclear. Here, we combine hybridization-based targeted capture14–16, multiplex PCR17,18 and high-throughput sequencing to generate 54 complete mammoth mitochondrial genomes, including 22 from temperate localities across Eurasia. We incorporate these into a globally extensive data set totalling 143 mammoth mitochondrial genomes sampled from across the northern hemisphere. We use a combined approach that incorporates both the deep paleontological record and more recent radiocarbon dates to calibrate the evolutionary rate, and infer the most comprehensive mammoth mitochondrial phylogeny to date. Results Using hybridization
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